Báo cáo thú y: "An assessment of soybeans and other vegetable proteins as source of salmonella contamination in pig production" ppsx

RESEARC H Open Access
An assessment of soybeans and other vegetable
proteins as source of salmonella contamination in
pig production
Martin Wierup
1*
, Per Häggblom
2
Abstract
Background: The impact of salmonella contaminated feed ingredients on the risk for spreading salmonella to pigs
was assessed in response to two incidences when salmonella was spread by feed from two feed mills to 78 swine
producing herds.
Methods: The assessment was based on results from the salmonella surveillance of feed ingredients before
introduction to feed mills and from HACCP - based surveillance of the feed mills. Results from the mills of the
Company (A) that produced the salmon ella contaminated feed, were by the Chi. Square test compared to the
results from all the other (B - E) feed producers registered in Sweden. Isolated serovars were compared to serovars
from human cases of salmonellosis.
Results: Salmonella (28 serovars) was frequently isolated from imported consignments of soybean meal (14.6%)
and rape seed meal (10.0%). Company A largely imported soybean meal from crushing plants with a history of
unknown or frequent salmonella contamination. The risk for consignments of vegetable proteins to be salmonella
contaminated was 2.4 times (P < 0.0006) larger for A when compared to the mills of the other companies which
largely were supplied by soybean meal from a crushing plant with a low risk for salmonella contamination. Also
the level of feed mill contamination of salmonella was higher for feed mills belonging to Company A in
comparison to the other companies before and also after heat treatment. Four (10.5%) of the 38 serovars isolated
from feed ingredients (28) and feed mills (10) were on the EU 2007 top ten list of human cases of salmonellosis
and all but eight (78.9%) on a 12 year list (1997-2008) of cases of human salmon ellosis in Sweden.
Conclusions: Salmonella contaminated feed ingredients are an important source for introducing salmonella into
the feed and food chain. Effective HACCP-based control and associated corrective actions are required to prevent
salmonella contamination of feed. Efforts should be taken to prevent salmonella contamination already at the
crushing plants. This is challenge for the EU - feed industry due to the fact that 98% of the use of soybean/meal,
an essential feed ingredient, is imported from crushing plants of third countries usually with an unknown

salmonella status.
Background
In the EU, salmonello sis and campylobacteriosis are the
most frequently occurring zoonotic infection in humans.
Up to approximately 200 000 human cases are annually
reported for eac h of t hese infections in the EFSA zoo-
noses reports since 2004 [1]. Other remaining zoonoses
are reported to occur in much lower numbers,
approximately: Yersiniosis (9000 cases), VTEC (2900),
Listeriosis (1500), Echinococcosis (800), Tricinillosis
(800), Brucellosis (500), Tuberc ulosis caused by M.
bovis (120) and rabies (<5). The majority of the food
borne outbreaks reported in EU a re also caused by sal-
monella and e.g. of the food borne outbreaks reported
during 2005 (5311 outbreaks involving approx. 47251
human cases out of which 5330 hospitalised and 24
deaths) salmonella was the most important causative
agent (64%), followed by Campylobacter (9%) and
viruses (6%) [2].
* Correspondence:
1
Department of Biomedical Sciences and Veterinary Public Health, Box 7009,
Swedish University of Agricultural Sciences, 75007 Uppsala, Sweden
Wierup and Häggblom Acta Veterinaria Scandinavica 2010, 52:15
/>© 2010 Wierup and Häggblom; licensee BioMe d Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribut ion License ( which permits unrestricted use, distribu tion, and
reproduction in any medium, provided the original work is properly cited.
In order to decrease the burden of salmonella infec-
tions focus have been given to the prevention of the
introduction of salmonella into the food chain through

the food animal production. In the EU, actions were pri-
marily directed to poultry producing eggs and meat.
Currently actions are planned to bring down the preva-
lence of salmonella conta mination in the swine produc-
tion in accordance with Reg ulation (EC No 2160 /2003).
So called baseline studies have been performed in all
Member States to obtain a more comparable estimate of
the prevalence of contamination in the Member States
[1]. In addition, EFSA has conducted different risk
assessments on how to reduce the prevalence of salmo-
nella in the swine production [3] as a base for those tar-
get levels for salmonella contamination that the EU
Commission will set according to the new food law
((EC) No 178/2002) that is in power since 2002. In this
respect attention has also been given to the importance
of salmonella contamination of animal feed as being the
first link of the animal derived food chain [4,5].
A striking example of the potential of animal feed as a
source of salmonella infections in humans occurred
when S. Agona emerged as a public health problem in
several countries due to the spread of contaminated
imported fish meal used in animal feed. In the United
States a rapid increase of human infection s with S.
Agona occurred from 1968 to 1972 [6] and a similar
increase of human infections with S. Agona occurred
simultaneously in European countries. Since t hen, S.
Agona is among the most prevalent serotypes in
humans e.g. in the USA, and it is estimated that the ser-
otype has caused more than one million human illnesses
in the USA alone since it was introduced into the food

chain [7].
It is difficult to evaluate the importance of feed as a
source o f salmonella infection in animals and it s subse-
quent spread to humans, when sever al serovars of sal-
monella simultaneously occur in different parts of the
food chain, which currently is the case in many Member
States of the EU [1]. In contrast it is easier to perform
such an assessment in a country with a low prevalence
of contamination in the animal food chain.
Against this background we present an assessment of
the possible impact of salmonella contaminated vegetable
protein as feed ingredients on the risk for spreading sal-
monella in animal feed production in Sweden, a country
which ha s demonstrated a very low prevalence of salmo-
nella in the animal food l production [1] and where data
since many years are available from the control of the feed
production [4]. The study was done during a two year per-
iod when salmonella was spread by feed from two feed
mills to 49 and 29 swin e producing herds respectively
[8,9]. Both feed mills belonged to the same company (A).
The salmonella contamination of high risk feed mate-
rials, when tested before introduction to the feed mills,
is presented as well as the result of HACCP-based con-
trol of salmonella contamination at different sampling
points in the production environment within the feed
mills. The results from Company (A) were compared
with results from all other commercial feed mills in
Sweden during the same period. In addition, the results
from of the HACCP control of feed mills from 2000 to
2005 as well as from two randomly selected earlier years

(1991 and 1997) is presented. The study is based on an
inquiry on behalf of Swedish Board of Agriculture [20].
Methods
1. Feed mills
The Swedish feed industry has undergone significant
changes to meet the rationalization in the farm sector
characterized by a dramatic decrease in nu mber of food
animal producing enterprises and to an overall decrease
ofthefeedvolumeproducedbyca15%duringthelast
10 years. The largest company (A) was operating 9 f eed
mills, while Company B which was running two fac-
tories and was joined to A by a business agreement.
Company C was a group running 4 feed mills. Company
D owned one feed mill and those under E comprised
several smaller enterprises. The relative volume of feed
produced by each group is indicated by their estimated
market share as presented in Table 1. During the period
of the study the mean size of Swedish feed mills
(volume produc ed per feed mill) was the second largest
of the EU member states a ccording to European Feed
Manufacturers Federation [10]. Pig feed is in most cases
produced in the same feed mill as poultry feed, however,
pig feed may also be produced in feed mills where cattle
feed is produced. The number of feed mills producing
pig feed was for Comp any A 5, B 1 and C 2. The num -
ber of production lines varies between the feed mills.
2. Control of high risk feed material
According to national legislation (SVS 2006:81) feed
materials are categorized according to risk for salmo-
nella contamination, and those feed ingredients found to

have a high risk have to be tested negative for salmo-
nella contamination before being used for feed produc-
tion. In practice they are not allowed to enter the feed
mill before a negative test result are at hand. Consign-
ments found to be salmonella contaminated are sub-
jected to a decontamination procedure by using organic
acids followed by re-testing with negative result. During
the period studied, the high risk feed materials used for
feed production intended to swine, involved soybean
meal, rape seed meal, pa lm kernel meal and maize/corn.
The products were imported to S weden by the feed
Wierup and Häggblom Acta Veterinaria Scandinavica 2010, 52:15
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companies. Each consignment was usually a shipload of
1200 - 2500 tonnes or trucks loading 30 tonnes.
3. HACCP control in feed mills
In line with the EU legislation, (EC) No 2160/2003 on
control of salmonella and other zoonotic agents, a
national control programme for feed was established in
Sweden 1993 (although not yet a harmonized demand
in the EU). In this legislation (SJVFS 2006:81) the fol-
lowing five critical control points in the processing line
were identified in feed mills ma nufacturing compound
feed for food producing animals:
1. Top of bin for final feed (compound feed).
2. Room for pellet coolers.
3. Top of pellet cooler.
4. Dust from the aspiration system (filter).
5. Intake pit/bot tom part of elevator for feed
materials.

At these critical control points dust samples or sweep-
ings are collected.
When poultry feed is produced, a minimum of one
environmental sample has to be taken at each of the
above five critical control points on a weekly basis and
checked for the absence of salmonella. When only non-
poultry feed is produced the corresponding requirement
is limited to control points 1 and 5. In addition to sur-
veillance o f the processing line, heat treatment of poul-
try feed is a requirement in the legislation. These
samples are taken by the operator and all samples have
to be sent to the National Veterinary Institute (SVA) for
analysis and control that the number of samples is in
accordance with the legislation. However, most opera-
tors normally take additional environmental samples on
a voluntary basis. When salmonella is detected further
serotyping is carried out.
The national legislation also prescribes the actions to
be taken when salmonella is found in feed mills.
According to the legislation the competent authority has
to be notified when salmonella is isolated after heat
treatment, and depending on location in the fe ed mill
and feed type the a ctions varies from further sampling
to assess the problem to immediate stop of production.
Cleaning and disinf ection as well as follow up proce-
dures are always carried out according to a plant speci-
fic cleaning programme that has to be in place. When
justified the competent authority (Swedish Board of
Agriculture) can modify these programmes.
4. Sampling and bacteriological methods

The s urveillance of feed ingredients is based on a sam-
pling procedure which takes into consideration an
uneven distribution of salmonella contamination and is
designed to detect a contamination in 5% of the batch
with 95% probability [11]. The size of the analytical
sample is 25 gram and usually 8 samples are analyzed;
each consisting of 10 pooled subsamples of 2.5 gram.
The detection of salmonel la from feed ingredients is
based on culture methods according to the NMKL-7 1
method [12]. The same method is also applied for the
analyses of samples in the HACCP control. Samples
taken when positive samples are identified can also be
analyzed a t other approved laboratories. Environmental
samples taken in addition to the legislation are usually
analyzed by industry laboratories.
In order to obtain information whether feed associated
serovars were identical to serovars in human cases of
salmonellosis a comparison was done with EFSA ten
most prevalent serovars from human cases of salmone-
losis in the EU (EFSA 2009). The data were also com-
pared with corresponding data from Sweden between
1997-2008 covering all serovars of salmonella reported
andsubtypedbyTheSwedishInstitute for Infectious
Table 1 Number of salmonella positive samples from the weekly environmental surveillance of the production line of
feed mills in Sweden - before heat treatment; and distribution of positive samples and estimated share of national
feed production between 1995 and 2005
Year/Feed producing company No. of salmonella positive samples before heat treatment
(% distribution of positive samples between companies for each
year)
Estimated share of national production

1995 1997 2000 2001 2002 2003 2004 2005 Total
A+B 36
(90%)
22
(82%)
45
(94%)
20
(95%)
17
(94%)
21
(66%)
7
(88%)
19
(90%)
187
(87%)
75%
C 4
(10%)
5
(18%)
2
(4%)
1
(5%)
1
(6%)

7
(22%)
0
(0%)
2
(10%)
22
(10%)
15%
D+E
1)
-0
(0%)
1
(2%)
0
(0%)
0
(0%)
4
(12%)
1
(12%)
0
(0%)
6
(3%)
10%
Total 40 27 48 21 18 32 8 21 215 100%
1) Includes also technically less advanced smaller factories

Wierup and Häggblom Acta Veterinaria Scandinavica 2010, 52:15
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Disease Control (Ivarsson 2009; personal
communication).
5. Statistical analyses
Statistical analyses were carried out by the Chi. Square
test [13].
Results
Imported high risk feed material
In 2004 and 2005 a total of 795 (year/no consignments:
2004/398 and 2005/397) consignments of vegetable pro-
teins, mostly soybean and rapeseed meal, were imported
to Sweden. A total 5250 pooled samples were investi-
gated for salmonella contamination and 131 (2.5%) of
the samples and 83 (10.4%) of the consignments were
contaminated. W hen result was split into different pro-
ducts 14.6% and 10.0% of imported consignments of
soybean meal and rapeseed meal, respectively, were
found to be contaminated (Figure 1). It should be noted
that Figure 1 in contrast to Figure 2, does not include
soybean meal which was tested negative for salmonella
before export from a Scandinavian source, at a volume
corresponding to the mean size of approximately 46
shiploads.
The soybean products were imported either from a
Scandinavian crushing plant with a long term documen-
ted quality assurance for freedom of salmonella contam-
ination or from different producers in South America,
usually from Brazil The latter soybean meal was
imported by two feed producing companies (A and B)

and the salmonella contaminated consignments shown
in Figure 2 were also concentrated to these two compa-
nies. The difference between A and B is likely to reflect
that they used soy or rape seed meal from different pro-
ducers. In 2004 Company A imported t he majority o f
the soybean meal from South America and 29 out of
144 imported consignments were contaminated by sal-
monella (20.1%) based on the sampling methods used.
In 2004 54% of the investigated consignments were
imported by Company A and contained 90% (p <
0.0001) of the salmonella contaminated samples taken
from the v egetable proteins imported, and 71% of the
sero vars (p < 0.01). In 2004 16.0% and in 2005 10.7% of
the c onsignments imported by A were found to be sal-
monella contaminated. The risk for imported consign-
ments to be salmonella contaminated in both 2004 and
2005 was 2.4 times (P < 0.0006) larger for consignments
imported by A than by the other importing feed mills.
Figure 1 Salmonella contamination of feed proteins importedtoSwedenbyfeedfactories2004-05. Number of consignments of
vegetable feed ingredients imported to Sweden from non Scandinavian sources during 2004-2005 and percent of these found contaminated by
salmonella in control before introduction in feed mills.
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2. HACCP control within feed mills
The result of the manda tory environmental samples
taken at different control points before and after heat
treatment is presented in Table 1 and 2. In addition to
2004-2005, Table 1 a nd Table 2 also include resu lts
from a ten year period to get a wider perspective of the
contamination rate. In these table s all feed mills belong-

ing to Company A also includes Company B because of
the business agreement that started 2000) and because
data were initially presented as a total . However, Com-
pany B operated its HACCP control as before that
agreement which is highlighted below. Th e proportions
of salmonella contaminated samples from feed mills
from A and B before and after heat treatment (87%;
Table 1 and 86%; Table 2 respectively), were larger than
expected by their market share (75%), during all the ten
years studied. In contrast, the opposite situation was
found for the feed mills belonging to C-E. The results
from the samples taken a fter heat treatment were of
particular interest. None of those samples from the fac-
tories belong to the C group were found to be contami-
nated. The salmonella contamination after heat
treatment in group D included non traditional small
feed mills some of which closed down as a result of
sanitation procedures following the contamination.
As a further elucidation of the efficiency of the
HACCP control, data from A and B feed mills were
separated (Tables 3 and 4) and studied 2000 - 2005. It
can be seen that salmonella contamination bef ore heat
treatment occurred in factories of both companies
(Table 3). Feed mill of B periodically faced severe pro-
blems (years 2000, 2003 and 2005) with an in house
contamination of unknown origin, when up to 14 differ-
ent serovars of salmonella where detected per period. At
Company B, in contrast to A this contamination was
not detected after heat treatment (Table 4).
In Figure 3 is the summary result of environmental

surveillance for salmonella contamination (HACCP)
take n in Swedish feed mills from 1991 to 2005. The fig-
ure also includes samples taken as a follow up proce-
dure when salmonella contamination was identified. In
spite that the commercial feed production roughly has
decreased by approximately 10% during the period the
number of samples has increased from 4000 to 8000
samples per year. During the same period the propor-
tion of salmonella positive samples had decreased from
2% to < 0.5%.
Salmonella serovars
A total of 28 diff erent serovars of salmonella, including
one non typeable strain, were isolated from vegetable
proteins imported to Sweden during 2004-2005. These
serovars were in alphabetic ord er: S.Adelaide,S. Agona,
S.Anatum,S. Bere, S.Cerro,S. Cubana, S. Gaminara, S.
Figure 2 Salmonella contamination of feed proteins imported to Sweden by feed factories 2004- 05. Total number of consignmen ts of
vegetable feed ingredients imported to Sweden (including from Scandinavian sources) by different feed producing companies during 2004-2005
and the proportion found contaminated by salmonella in control before introduction in feed mills.
Wierup and Häggblom Acta Veterinaria Scandinavica 2010, 52:15
/>Page 5 of 9
Glowcester, S. Havana, S.Infantis,S.KentuckyS.Lex-
ington, S. Livingstone,S. Llandoff, S. Mbandaka, S More-
head, S.Muenster,S. Obogu, S.Ohio,S. Panama, S.
Reading,S. Rissen, S. Senftenberg, S. Tennessee, S.
Tabligo, S. Typhimurium (not phage typed) and S.Yor-
uba. When adding thos e serovars isolated in 2000, 2003
and 2005 in the HACCP c ontrol in the feed mill of
Company B (Table 3, data from the remaining factories
and years not present) an additional 10 new serovars

were isolated. These were: S. Bredeney, S. C orvallis, S.
Glostrup, S.Kingston,S. Schwarzengrund,S.Typhimur-
ium phage type 41, S. Typhimurium phage type 193, S.
Oranienburg, S. Umbilio and S. Ouakam.
Four (10.5%) of the serovars isolated (S.Agona,S.
Infantis, S. Kentucky and S. Typhimurium-included at
least two different strains) were identical to the 10 most
common isolates of human cases of salmonellosis in the
EU [1] and out of the 38 feed associated serovars identi-
fied 78.9% or all but 8 (S. Bere, S. Glowcester , S. Lland-
off, S. Morehead S. Obogu, S. Ouakam,, S. Tabligo and
S. Yoruba) had been isolated from human cases of sal-
monellosis diagnosed in Sweden 1997-2008.
Discussion
Salmonella was frequently isolated from consignments
of vegetable proteins used as feed ingredients, in parti-
cular from soybean meal (14.6%) and rape seed meal
(10.0%) (Figure 2). When the majority of the imported
soy was from South America 20.1% of the consignments
were contaminated by salmonella (data not shown).
Even higher levels, up to 30%, have regularly been found
in the Sweden when high risk ingredients from South
America are tested before introduction to the feed mills
[14]. The frequent isolation of salmonella from vegetable
proteins is in agreement with several observations from
different countries. In a Dutch report 3.2% an d 6.7% of
Brazilian extracted soybeans were found positive for sal-
monella during 2002 and 2003 respectively [15]. In a
recent comprehensive study based on an annual exami-
nation of up to 80,000 lots of feed, Kwiatek et.al [16]

report that in Poland up to 15.0% and 15.4% of
imported lots of soy and rape seed were respectively sal-
monella contaminated in 2005-2007. Corresponding
data for products produced in Poland were 6.3% and
7.7%. In summary, it can be concluded that the oil seed
feed ingredients are often contaminated by salmonella
although it is difficult to compare the level of contami-
nation between different studies b ecause the results
depend on the sampling and culture techniques applied.
The study also demonstrates that the vegetable pro-
teinsusedbyCompanyAsignificantlymoreoftenwere
salmonella contaminated, and also harboured a signifi-
cantly larger number of different serovars, than feed
ingredients used by the remaining companies. This
Table 2 Number of salmonella positive samples from the weekly environmental surveillance of the production line of
feed mills in Sweden - after heat treatment; and distribution of positive samples and estimated share of national feed
production between 1995 and 2005
Year/feed producing company No. of salmonella positive samples after heat treatment Estimated share of national production
1995 1997 2000 2001 2002 2003 2004 2005 Total
(%)
2)
A+B 7 7 7 1 2 7 0 1 32 (86%) 75%
C 00000000 0
(0%)
15%
D+E
1)
10012100 5
(14%)
10%

Total 87724801 37
(100%)
100%
1) Include also non - traditional” smaller factories
2)% distribution of positive samples between companies for each year
Table 3 Number of salmonella positive samples from environmental weekly surveillance of the production line -
before heat treatment of feed mills of A and B using largely the same feed ingredients
Year/feed producing company Number of salmonella positive
samples collected before heat treatment
Total
2000 2001 2002 2003 2004 2005
A 32 17 14 10 7 3 83
B 13
1)
3311
2)
016
3)
46
1. Nine different serovars of salmonella isolated.
2. Nine different serovars of salmonella isolated.
3. 14 different serovars of salmonella isolated.
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reflects that Company A largely had replaced a supplier
of soy products with a high level of quality control for
freedom of salmonella with imports from South Amer-
ica. This was the case particularly in2004 when 29 out
of 144 imported consignments were contaminated by
salmonella (20.1%, data not shown). As a comparison

the mills of Company C, which bought all soy products
from a supplier with a high salmonella quality assur-
ance, none (0%) of the imported 46 consignments were
salmonella contaminated during that year (data not
shown).
The higher exposure to salmonella by feed ingredient s
to feed mills of Company A, in comparison to the mills
of Company C - E, was reflected in an increased in
house contamination of salmonella of the mills of Com-
pan y A, also when including Company B. The contami -
nation was detected before the heat treatment (Tab le 1)
but more severe also after that step (the clean area). No
salmonella contamination was detected after heat
treatment Company C feed mills in spite the fact that
salmonella contamination occurred before that step.
The r esults from the feed mills of Company B are of
special interest. In spite o f periods with heavy salmo-
nella contamination during three years (2000, 2003 and
2005) before the heat treatment process, the HACCP
surveillance could never detect any salmonella contami-
nation after that step in contrast to in the feed mills of
Company A (Table 3 and 4). This demonstrates that
management procedures, supported by HACCP-control
and heat treatment can prevent salmonella contamina-
tion of feed ingredients to be transmitted to the clean
areas (after heat treatment) of the feed mills and thereby
to the compounded feed, although factors like the
design of the feed mills and contamination from other
external environmental sources can influence the r esult.
It is logical to assume that when the salmonella contam-

ination in incoming feed ingredients increase to a cer-
tain level, the feed mill environment may become
Table 4 Number of salmonella positive samples from environmental weekly surveillance of the production line - after
heat treatment of feed mills of A and B using largely the same feed ingredients
Year/feed producing company Number of salmonella positive samples collected after heat treatment Total
2000 2001 2002 2003 2004 2005
A 71270118
B 0000000
0
2000
4000
6000
8000
10000
12000
1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005
0.0%
0.5%
1.0%
1.5%
2.0%
2.5%
No. samples
% positive
Figure 3 Number of environmental samples of the production line (HACCP - control) taken voluntarily (1991-1992) and according to
legal requirements (1993-2005) for salmonella surveillanceof registered/approved feed mills in Sweden.
Wierup and Häggblom Acta Veterinaria Scandinavica 2010, 52:15
/>Page 7 of 9
contaminated which increases the risk for the contami-
nation of the compounded feed. It is therefore also logi-

cal to assume that the feed mills of Company A, in spite
of decontamination by organic acids, could not manage
the relatively high level of salmonella contamination. It
is also plausible to consider that this is the underlying
reason why salmonella was transmitted to pigs fed by
feed produced by its feed mills [8,9].
The feed ingredients found salmonella positive were
treated by organic acids for decontamination purposes.
This is a metho d which can reduce the contamination of
salmonella [17] although the method might mask the
detection of surviving microbes [18]. Even though the
acid treated consignments were not allowed to enter feed
mill until a negati ve test procedure, the decontamination
process cannot be considered as a guarantee for freedom
from salmonella but instead that the level of contamina-
tion has been brought under t he detection level of the
test method applied. The Swedi sh legislation therefore
prescribes that feed including feed ingredients that have
undergone decontamination by other methods than heat
treatment must be heat treated. Suitable technical equip-
ment and the layout of the producti on line is also essen-
tial for production of safe feed. Aspiration of dust is
essential in all feed production and particularly when
contaminated ingredients are introduced in the mill. The
importance of a continuous monitoring for salmonella
contamination of the feed production within a HACCP
designed control, and the implementation of associa ted
corrective actions when such contamination is detected,
is in Sweden found t o be of basic importan ce to prevent
the introduction of salmonella into the food animal pro-

duction and subsequently to the food chain [4]. Although
the design of the feed mill may influence the number of
samples required for an effective HACCP-surveillance,
this study interestingly also f ound (data not shown) that
in all the feed mills the in house monitoring for poultry
feed was generally more intensive than was legally
required. One Company (B) applied a more intensive
heat treatment for poultry feed and in Company A up to
14 weekly environmental samples were taken in the poul-
try feed production, close to three times more than those
five samples which are the minimum legal requirem ent.
Long term documentation also demonstrates that the
poultry feed (including feed from Company A) by the
methods applied to prevent salmonella contamination,
since the mid 1980-ies is virtually free from salmonella.
The latter is indicated by the very low incidence of sal-
monella in the broiler p roduction when each flock is
tested before slaughter [ 1]. In Sweden the latter control,
which on a volu ntary basis started 1970, became manda-
tory 1984 in response to the spread of salmonella by feed
[19,20]. It is thus justified to recommend that feed to all
food animal species is treated equally.
The reason why so many as 28 serovars during a two
year period were isolated from imported vegetable pro-
teins is unknown. One explanation is that it can be the
result of previous incidences contaminations of the
crushing plants which not were elimin ated but instead
has been e stablishe d as an in house contamination that
can pop up periodically. Experiences from Denmark
have demonstrated that in some crushi ng pl ants certain

serovars of salmonella may persist for several years in
the premises [21]. Similar experiences are gained in
Sweden, e.g. the feed mill of Company B (Table 3).
Largely, the same serovars which were isolated from
the feed ingredients, were re isolated in the monitoring
of the feed mills (results not shown) thus demonstrating
the spread of the contamination from the feed ingredi-
ents to the feed m ills. If the feed mills cannot eliminate
this contamination or ensure that it is not contaminat-
ing the compounded feed, a further spread to the food
animals will occur which initiated this study [8,9]. At
present there is a similar outbreak in the Southern part
of Sweden where S. Typhimurium is considered to have
spread from feed to animals, to the environment, to
food and also to humans (Lahti 2009; personal
communication).
Animals are thus infected per orally by salmonella
contaminated feed in the same way as humans are
infected by salmonella contaminated food. If the feed
ingredients also include serovars which are known to
have a preference for infecting humans as indicated by
EFSA statistics [1] their occurrence in feed is also a
threat to human health. In this study four (10.5%) of the
38 feed asso ciated serovars isolated were included in the
top ten list of isolates from human confirmed cases of
salmonellosis in the EU [1]. In addition 76.3% out of the
feed associated strains had been isolated from human
cases of salmonellosis in Sweden. These finding require
a further study and cannot be used a cause rel ationship
with the salmone lla isolated from feed ingredients and

feed mills in this study. However, the results contradict
the often used argument against the need for preventing
salmonella contamination of feed by saying that feed
associated serovars are considered usually to be non-
pathogenic to humans Instead the result is in line with
conclusions by EFSA that all serovars are potentially
pathogenic to humans [5].
Insummarythereisastrongreasontopreventthe
introduction of salmonella into animal feed and efforts
should focus on the crushing plants as the primary
source for such introduction to the feed mills. The
Scandinavian crushing plant mentioned in this study
had not the capacity to supply all feed mills in Sweden.
Some feed companies therefore have to buy from
unknown sources with high risk for salmonella contami-
nation like Company A of this study. The same
Wierup and Häggblom Acta Veterinaria Scandinavica 2010, 52:15
/>Page 8 of 9
challenging situation applies for whole EU due to the
fact that 98% of soybeans or soybean meal is imported
from third countries [10].
Acknowledgements
Thanks to senior officer Stig Widell, Swedish Board of Agricultural, for
valuable advice on the manuscript in relation to the Swedish legislation and
official control of salmonella.
Author details
1
Department of Biomedical Sciences and Veterinary Public Health, Box 7009,
Swedish University of Agricultural Sciences, 75007 Uppsala, Sweden.
2

Department of Chemistry, Animal feed and Environment, National
Veterinary Institute, 75189, Uppsala Sweden.
Authors’ contributions
The study and field work was designed, done and written by MW [20] based
largely on industry laboratory data. Data from HACCP surveillance and from
other official data from PH and from Swedish Board of Agriculture. Both
authors revised the final manuscript.
Competing interests
The authors declare that they have no competing interests.
Received: 18 December 2009
Accepted: 17 February 2010 Published: 17 February 2010
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doi:10.1186/1751-0147-52-15
Cite this article as: Wierup and Häggblom: An assessment of soybeans
and other vegetable proteins as source of salmonella contamination in
pig production. Acta Veterinaria Scandinavica 2010 52:15.
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